Rifaximin improves Clostridium difficile toxin A-induced toxicity in Caco-2 cells by the PXR-dependent TLR4/MyD88/NF-κB pathway

Frontiers in Pharmacology

Volumn 7, Issue MAY, 2016, Pages

  Esposito, Giuseppe ^a   Nobile, Nicola ^a   Gigli, Stefano ^a   Seguella, Luisa ^a   Pesce, Marcella ^b   d'Alessandro, Alessandra ^b   Bruzzese, Eugenia ^b   Capoccia, Elena ^a   Steardo, Luca ^a   Cuomo, Rosario ^b   Sarnelli, Giovanni ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Caco 2 cells; Clostridium difficile toxin A; Pregnane X receptor; Pseudomembranous colitis; Rifaximin

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KETOCONAZOLE; MYELOID DIFFERENTIATION FACTOR 88; OCCLUDIN; PREGNANE X RECEPTOR; PROTEIN BAX; PROTEIN ZO1; RIFAXIMIN; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1;

APOPTOSIS; ARTICLE; CACO 2 CELL LINE; CELL PROTECTION; CELL VIABILITY; CLOSTRIDIUM DIFFICILE INFECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSEPITHELIAL RESISTANCE;

EID: 84974533500     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2016.00120     Document Type: Article

References (33)

1. Akira, S., and Hoshino, K. (2003). Myeloid differentiation factor 88-dependent and-independent pathways in toll-like receptor signaling. J. Infect. Dis. 187, S356-S363. doi: 10.1086/374749
2. Cash, B. D., Lacy, B. E., Rao, T., and Earnest, D. L. (2016). Rifaximin and eluxadoline-newly approved treatments for diarrhea-predominant irritable bowel syndrome: what is their role in clinical practice alongside alosetron? Expert Opin. Pharmacother. 17, 311-322. doi: 10.1517/14656566.2016.1118052
3. Cheng, J., Shah, Y. M., Ma, X., Pang, X., Tanaka, T., Kodama, T., et al. (2010). Therapeutic role of rifaximin in inflammatory bowel disease: clinical implication of human pregnane X receptor activation. J. Pharmacol. Exp. Ther. 335, 32-41. doi: 10.1124/jpet.110.170225
4. Dou, W., Mukherjee, S., Li, H., Venkatesh, M., Wang, H., Kortagere, S., et al. (2012). Alleviation of gut inflammation by Cdx2/Pxr pathway in a mouse model of chemical colitis. PLoS ONE 7:e36075. doi: 10.1371/journal.pone.0036075
5. Ebigbo, A., and Messmann, H. (2013). Challenges of Clostridium difficile infection. Med. Klin. Intensivmed. Notfmed. 108, 624-627. doi: 10.1007/s00063-013-0258-7
6. Fanning, A. S., Jameson, B. J., Jesaitis, L. A., and Anderson, J. M. (1998). The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273, 29745-29753. doi: 10.1074/jbc.273.45.29745
7. Huynh-Delerme, C., Huet, H., Noel, L., Frigieri, A., and Kolf-Clauw, M. (2005). Increased functional expression of P-glycoprotein in Caco-2 TC7 cells exposed long-term to cadmium. Toxicol. In Vitro 19, 439-447. doi: 10.1016/j.tiv.2004.08.003
8. Jodlowski, T. Z., Oehler, R., Kam, L. W., and Melnychuk, I. (2006). Emerging therapies in the treatment of Clostridium difficile-associated disease. Ann. Pharmacother. 40, 2164-2169. doi: 10.1345/aph.1H340
9. Kawai, T., and Akira, S. (2007). Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13, 460-469. doi: 10.1016/j.molmed.2007.09.002
10. Layer, P., and Andresen, V. (2010). Review article: rifaximin, a minimally absorbed oral antibacterial, for the treatment of travellers' diarrhoea. Aliment. Pharmacol. Ther. 31, 1155-1164. doi: 10.1111/j.1365-2036.2010.04296.x
11. Leffler, D. A., and Lamont, J. T. (2015). Clostridium difficile infection. N. Engl. J. Med. 372, 1539-1548. doi: 10.1056/NEJMra1403772
12. Ma, X., Shah, Y. M., Guo, G. L., Wang, T., Krausz, K. W., Idle, J. R., et al. (2007). Rifaximin is a gut-specific human pregnane X receptor activator. J. Pharmacol. Exp. Ther. 322, 391-398. doi: 10.1124/jpet.107.121913
13. Madara, J. L., Stafford, J., Barenberg, D., and Carlson, S. (1988). Functional coupling of tight junctions and microfilaments in T84 monolayers. Am. J. Physiol. 254, G416-G423.
14. Mani, S., Dou, W., and Redinbo, M. R. (2013). PXR antagonists and implication in drug metabolism. Drug Metab. Rev. 45, 60-72. doi: 10.3109/03602532.2012.746363
15. Mencarelli, A., Migliorati, M., Barbanti, M., Cipriani, S., Palladino, G., Distrutti, E., et al. (2010). Pregnane-X-receptor mediates the anti-inflammatory activities of rifaximin on detoxification pathways in intestinal epithelial cells. Biochem. Pharmacol. 80, 1700-1707. doi: 10.1016/j.bcp.2010.08.022
16. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63. doi: 10.1016/0022-1759(83)90303-4
17. O'Neill, L. A., Dunne, A., Edjeback, M., Gray, P., Jefferies, C., and Wietek, C. (2003). Mal and MyD88: adapter proteins involved in signal transduction by Toll-like receptors. J. Endotoxin Res. 9, 55-59. doi: 10.1177/09680519030090010701
18. Pawlowski, J., and Kraft, A. S. (2000). Bax-induced apoptotic cell death. Proc. Natl. Acad. Sci. U.S.A. 97, 529-531. doi: 10.1073/pnas.97.2.529
19. Rakoff-Nahoum, S., and Medzhitov, R. (2009). Toll-like receptors and cancer. Nat. Rev. Cancer 9, 57-63. doi: 10.1038/nrc2541
20. Rupnik, M., Wilcox, M. H., and Gerding, D. N. (2009). Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526-536. doi: 10.1038/nrmicro2164
21. Sanchez-Delgado, J., and Miquel, M. (2015). Role of rifaximin in the treatment of hepatic encephalopathy. Gastroenterol. Hepatol. 2015, 3. [Epub ahead of print].
22. Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T., et al. (2005). Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6, 1087-1095. doi: 10.1038/ni1255
23. Scarpignato, C., and Pelosini, I. (2005). Rifaximin, a poorly absorbed antibiotic: pharmacology and clinical potential. Chemotherapy 51, 36-66. doi: 10.1159/000081990
24. Scarpignato, C., and Pelosini, I. (2006). Experimental and clinical pharmacology of rifaximin, a gastrointestinal selective antibiotic. Digestion 73, 13-27. doi: 10.1159/000089776
25. Smutny, T., Mani, S., and Pavek, P. (2013). Post-translational and post-transcriptional modifications of pregnane X receptor (PXR) in regulation of the cytochrome P450 superfamily. Curr. Drug Metab. 14, 1059-1069. doi: 10.2174/1389200214666131211153307
26. Surawicz, C. M., and McFarland, L. V. (1999). Pseudomembranous colitis: causes and cures. Digestion 60, 91-100. doi: 10.1159/000007633
27. Terc, J., Hansen, A., Alston, L., and Hirota, S. A. (2014). Pregnane X receptor agonists enhance intestinal epithelial wound healing and repair of the intestinal barrier following the induction of experimental colitis. Eur. J. Pharm. Sci. 55, 12-19. doi: 10.1016/j.ejps.2014.01.007
28. Waltz, P., and Zuckerbraun, B. (2016). Novel therapies for severe Clostridium difficile colitis. Curr. Opin. Crit. Care doi: 10.1097/MCC.0000000000000282 [Epub ahead of print].
29. Wan, Y. C., Li, T., Han, Y. D., Zhang, H. Y., Lin, H., and Zhang, B. (2015). Effect of pregnane xenobiotic receptor activation on inflammatory bowel disease treated with rifaximin. J. Biol. Regul. Homeost. Agents 29, 401-410.
30. Wells, C. L., van de Westerlo, E. M., Jechorek, R. P., Haines, H. M., and Erlandsen, S. L. (1998). Cytochalasin-induced actin disruption of polarized enterocytes can augment internalization of bacteria. Infect. Immun. 66, 2410-2419.
31. Westphal, D., Dewson, G., Czabotar, P. E., and Kluck, R. M. (2011). Molecular biology of Bax and Bak activation and action. Biochim. Biophys. Acta 1813, 521-531. doi: 10.1016/j.bbamcr.2010.12.019
32. Zhang, B., Xie, W., and Krasowski, M. D. (2008). PXR: a xenobiotic receptor of diverse function implicated in pharmacogenetics. Pharmacogenomics 9, 1695-1709. doi: 10.2217/14622416.9.11.1695
33. Zhang, J., Ding, L., Wang, B., Ren, G., Sun, A., Deng, C., et al. (2015). Notoginsenoside R1 attenuates experimental inflammatory bowel disease via pregnane X receptor activation. J. Pharmacol. Exp. Ther. 352, 315-324. doi: 10.1124/jpet.114.218750